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Cuticular proteins, in conjunction with chitin, compose the insect exoskeleton, and play a key role in the growth, development, and molting of insects. However, the specific functions of most cuticular protein genes in the growth, development, and reproductive processes of the pea aphid (Acyrthosiphon pisum) remain unclear. In this study, we have identified six cuticular protein genes in the pea aphid, namely ApCP7, ApCP10, ApCP19, ApCP19.8-like, ApCP35 and ApCP62. We found that the expression levels of six genes were highly expressed during the adult stage, and except for ApCP10, which is highly expressed in the pea aphid cuticle, other genes were highly expressed in the ovaries. Subsequently, we observed that the survival rate and fecundity of pea aphid were significantly lower than those of the control group after silencing ApCP7 and ApCP62 through RNA interference. Furthermore, when ApCP7 transcript levels were reduced, aphid encountered difficulties in molting, were smaller in body size, and exhibited a darker body color. These results indicate that ApCP7 and ApCP62 are involved in the development and reproduction of pea aphid, and could be used as RNAi targets for controlling pea aphid.

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Hesperidin is a highly bioactive natural flavonoid whose role in ecological interactions is poorly known. In particular, the effects of hesperidin on herbivores are rarely reported. Flavonoids have been considered as prospective biopesticides; therefore, the aim of the present study was to examine the influence of hesperidin on the host plant selection behavior of three aphid (Hemiptera: Aphididae) species: Acyrthosiphon pisum Harrris, Rhopalosiphum padi (L.), and Myzus persicae (Sulz.). The aphid host plants were treated with 0.1% and 0.5% ethanolic solutions of hesperidin. Aphid probing behavior in the no-choice experiment was monitored using electropenetrography and aphid settling on plants in the choice experiment was recorded. The results demonstrated that hesperidin can be applied as a pre-ingestive, ingestive, and post-ingestive deterrent against A. pisum, as an ingestive deterrent against R. padi, and as a post-ingestive deterrent against M. persicae using the relatively low 0.1% concentration. While in A. pisum the deterrent effects of hesperidin were manifested as early as during aphid probing in peripheral plant tissues, in M. persicae, the avoidance of plants was probably the consequence of consuming the hesperidin-containing phloem sap.

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Soil rhizobia promote nitrogen fixation in legume hosts, maximizing their tolerance to different biotic stressors, plant biomass, crop growth, and yield. While the presence of soil rhizobia is considered beneficial for plants, few studies have assessed whether variation in rhizobia abundance affects the tolerance of legumes to stressors. To address this, we assessed the effects of variable soil rhizobia inoculum concentrations on interactions between a legume host (Pisum sativum), a vector insect (Acyrthosiphon pisum), and a virus (Pea enation mosaic virus, PEMV). We showed that increased rhizobia abundance reduces the inhibitory effects of PEMV on the nodule formation and root growth in 2-week-old plants. However, these trends were reversed in 4-week-old plants. Rhizobia abundance did not affect shoot growth or virus prevalence in 2- or 4-week-old plants. Our results show that rhizobia abundance may indirectly affect legume tolerance to a virus, but effects varied based on plant age. To assess the mechanisms that mediated interactions between rhizobia, plants, aphids, and PEMV, we measured the relative expression of gene transcripts related to plant defense signaling. Rhizobia concentrations did not strongly affect the expression of defense genes associated with phytohormone signaling. Our study shows that an abundance of soil rhizobia may impact a plant's ability to tolerate stressors such as vector-borne pathogens, as well as aid in developing sustainable pest and pathogen management systems for legume crops. More broadly, understanding how variable rhizobia concentrations can optimize legume-rhizobia symbiosis may enhance the productivity of legume crops.

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Plants simultaneously interact with belowground symbionts such as arbuscular mycorrhizal (AM) fungi and aboveground antagonists such as aphids. Generally, plants gain access to valuable resources including nutrients and water through the AM symbiosis and are more resistant to pests. Nevertheless, aphids' performance improves on mycorrhizal plants, and it remains unclear whether a more nutritious food source and/or attenuated defenses are the contributing factors. This study examined the shoot and root transcriptome of barrel medic (Medicago truncatula Gaertn.) plants highly colonized by the AM fungus Rhizophagus irregularis (Blaszk., Wubet, Renker, and Buscot) C. Walker and A. Schüßler (Glomerales: Glomeraceae) and exposed to 7 days of mixed age pea aphid (Acyrthosiphon pisum (Harris)) herbivory. The RNA-seq samples chosen for this study showed that aphids were heavier when fed mycorrhizal plants compared to nonmycorrhizal plants. We hypothesized that (i) insect-related plant defense pathways will be downregulated in shoots of mycorrhizal plants with aphids compared to nonmycorrhizal plants with aphids; (ii) pathways involved in nutrient acquisition, carbohydrate-related and amino acid transport will be upregulated in shoots of mycorrhizal plants with aphids compared to nonmycorrhizal plants with aphids; and (iii) roots of mycorrhizal plants with aphids will exhibit mycorrhiza-induced resistance. The transcriptome data revealed that the gene repertoire related to defenses, nutrient transport, and carbohydrates differs between nonmycorrhizal and mycorrhizal plants with aphids, which could explain the weight gain in aphids. We also identified novel candidate genes that are differentially expressed in nonmycorrhizal plants with aphids, thus setting the stage for future functional studies.

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The main aim of this study was to understand the regulation of the biosynthesis of phytohormones as signaling molecules in the defense mechanisms of pea seedlings during the application of abiotic and biotic stress factors. It was important to identify this regulation at the molecular level in Pisum sativum L. seedlings under the influence of various concentrations of lead-i.e., a low concentration increasing plant metabolism, causing a hormetic effect, and a high dose causing a sublethal effect-and during feeding of a phytophagous insect with a piercing-sucking mouthpart-i.e., pea aphid (Acyrthosiphon pisum (Harris)). The aim of the study was to determine the expression level of genes encoding enzymes of the biosynthesis of signaling molecules such as phytohormones-i.e., jasmonates (JA/MeJA), ethylene (ET) and abscisic acid (ABA). Real-time qPCR was applied to analyze the expression of genes encoding enzymes involved in the regulation of the biosynthesis of JA/MeJA (lipoxygenase 1 (LOX1), lipoxygenase 2 (LOX2), 12-oxophytodienoate reductase 1 (OPR1) and jasmonic acid-amido synthetase (JAR1)), ET (1-aminocyclopropane-1-carboxylate synthase 3 (ACS3)) and ABA (9-cis-epoxycarotenoid dioxygenase (NCED) and aldehyde oxidase 1 (AO1)). In response to the abovementioned stress factors-i.e., abiotic and biotic stressors acting independently or simultaneously-the expression of the LOX1, LOX2, OPR1, JAR1, ACS3, NCED and AO1 genes at both sublethal and hormetic doses increased. Particularly high levels of the relative expression of the tested genes in pea seedlings growing at sublethal doses of lead and colonized by A. pisum compared to the control were noticeable. A hormetic dose of lead induced high expression levels of the JAR1, OPR1 and ACS3 genes, especially in leaves. Moreover, an increase in the concentration of phytohormones such as jasmonates (JA and MeJA) and aminococyclopropane-1-carboxylic acid (ACC)-ethylene (ET) precursor was observed. The results of this study indicate that the response of pea seedlings to lead and A. pisum aphid infestation differed greatly at both the gene expression and metabolic levels. The intensity of these defense responses depended on the organ, the metal dose and direct contact of the stress factor with the organ.

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The neuropeptide pigment-dispersing factor (PDF) plays a pivotal role in the circadian clock of most Ecdysozoa and is additionally involved in the timing of seasonal responses of several photoperiodic species. The pea aphid, Acyrthosiphon pisum, is a paradigmatic photoperiodic species with an annual life cycle tightly coupled to the seasonal changes in day length. Nevertheless, PDF could not be identified in A. pisum so far. In the present study, we identified a PDF-coding gene that has undergone significant changes in the otherwise highly conserved insect C-terminal amino acid sequence. A newly generated aphid-specific PDF antibody stained four neurons in each hemisphere of the aphid brain that co-express the clock protein Period and have projections to the pars lateralis that are highly plastic and change their appearance in a daily and seasonal manner, resembling those of the fruit fly PDF neurons. Most intriguingly, the PDF terminals overlap with dendrites of the insulin-like peptide (ILP) positive neurosecretory cells in the pars intercerebralis and with putative terminals of Cryptochrome (CRY) positive clock neurons. Since ILP has been previously shown to be crucial for seasonal adaptations and CRY might serve as a circadian photoreceptor vital for measuring day length, our results suggest that PDF plays a critical role in aphid seasonal timing.

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Although phloem-feeding insects such as aphids can cause significant damage to plants, relatively little is known about early plant defenses against these insects. As a first line of defense, legumes can stop the phloem mass flow through a conformational change in phloem proteins known as forisomes in response to Ca2+ influx. However, specialized phloem-feeding insects might be able to suppress the conformational change of forisomes and thereby prevent sieve element occlusion. To investigate this possibility, we triggered forisome dispersion through application of a local heat stimulus to the leaf tips of pea (Pisum sativum), clover (Trifolium pratense) and broad bean (Vicia faba) plants infested with different pea aphid (Acyrthosiphon pisum) host races and monitored forisome responses. Pea aphids were able to suppress forisome dispersion, but this depended on the infesting aphid host race, the plant species, and the age of the plant. Differences in the ability of aphids to suppress forisome dispersion may be explained by differences in the composition and quantity of the aphid saliva injected into the plant. Various mechanisms of how pea aphids might suppress forisome dispersion are discussed.

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Many organisms exhibit phenotypic plasticity, in which developmental processes result in different phenotypes depending on their environmental context. Here we focus on the molecular mechanisms underlying that environmental response. Pea aphids (Acyrthosiphon pisum) exhibit a wing dimorphism, in which pea aphid mothers produce winged or wingless daughters when exposed to a crowded or low-density environment, respectively. We investigated the role of dopamine in mediating this wing plasticity, motivated by a previous study that found higher dopamine titres in wingless- versus winged-producing aphid mothers. In this study, we found that manipulating dopamine levels in aphid mothers affected the numbers of winged offspring they produced. Specifically, asexual female adults injected with a dopamine agonist produced a lower percentage of winged offspring, while asexual females injected with a dopamine antagonist produced a higher percentage of winged offspring, matching expectations based on the titre difference. We also found that genes involved in dopamine synthesis, degradation and signalling were not differentially expressed between wingless- and winged-producing aphids. This result indicates that titre regulation possibly happens in a non-transcriptional manner or that sampling of additional timepoints or tissues is necessary. Overall, our work emphasizes that dopamine is an important component of how organisms process information about their environments.

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Wing dimorphism in insects is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between dispersing and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that, while developing normally in winged-destined pea aphids, the wing disc in wingless-destined aphids degenerated 30-hr postbirth and that this degeneration was due to autophagy rather than apoptosis. Activation of autophagy in first instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. REPTOR2, associated with TOR signaling pathway, was identified by RNA-seq as a differentially expressed gene between the two morphs with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event that occurred exclusively in pea aphids on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR's canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. Co-suppression of TOR and REPTOR2 showed that dsREPTOR2 could mask the positive effect of dsTOR on autophagy, suggesting that REPTOR2 acted as a key regulator downstream of TOR in the signaling pathway. These results revealed that the TOR signaling pathway suppressed autophagic degradation of the wing disc in pea aphids by negatively regulating the expression of REPTOR2.

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The success of biological invasions ultimately relies on phenotypic traits of the invasive species. Aphids, which include many important pests worldwide, may have been successful invading new environments partly because they can maximize reproductive output by becoming parthenogenetic and losing the sexual phase of their reproductive cycle. However, invasive populations of aphids invading wide ranges can face contrasting environmental conditions and requiring different phenotypic strategies. Besides transitions in their reproductive cycle, it is only partially known which phenotypic traits might be associated to the invasion success of aphid populations in extended novel ranges. Here, we used four genotypes of the pea aphid Acyrthosiphon pisum from two localities in Chile to test for phenotypic specialization that might explain their establishment and spread in habitats exhibiting contrasting environmental conditions. We show that lineages living at a higher latitude with low temperatures show, in addition to facultative sexual reproduction, smaller body sizes, lower metabolic rates and a higher tolerance to the cold than the obligate asexual lineages living in a mild weather, at the expense of fecundity. Conversely, at higher temperatures only asexual lineages were found, which exhibit larger body sizes, higher reproductive outputs and consequently enhanced demographic ability. As a result, in conjunction with the reproductive mode, lineage specialization in physiological and life-history traits could be taken into account as an important strategy for populations of pea aphid to effectively invade extended novel ranges comprising different climatic conditions.

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Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiont Hamiltonella defensa confers protection against the parasitoid, Aphidius ervi, and Regiella insecticola protects against aphid-specific fungal pathogens, including Pandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virus A. pisum virus (APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont-free aphids and these costs were elevated in aphids also housing H. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids with R. insecticola. To our knowledge, R. insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of either R. insecticola or H. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont-mediated interactions.

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Pea aphid (Acyrthosiphon pisum) infestation leads to withering, reduced yield, and lower quality of the host plant. Arbuscular mycorrhizal (AM) fungi have been found to enhance their host plants' nutrient uptake, growth, and resistance to biotic stresses, including pathogen infection and insect pest infestation. Therefore, we evaluated the effects of AM fungus Rhizophagus intraradices on alfalfa defense responses to pea aphid infestation. Aphid infestation did not affect the colonization of AM fungus. The inoculation of AM fungus, on average, enhanced alfalfa catalase and the contents of salicylic acid and trypsin inhibitor by 101, 9.05, and 7.89% compared with non-mycorrhizal alfalfa, respectively. In addition, polyphenol oxidase activities significantly increased by six-fold after aphid infestation in mycorrhizal alfalfa. Moreover, the fungus significantly (p < 0.05) improved alfalfa shoot N content, net photosynthetic and transpiration rates, and shoot dry weight in aphid infected treatment. The aphid infestation changed the total volatile organic compounds (VOCs) in alfalfa, while AM fungus enhanced the contents of methyl salicylate (MeSA). The co-expression network analysis of differentially expressed genes (DEGs) and differentially expressed VOCs analysis showed that three DEGs, namely MS.gene23894, MS.gene003889, and MS.gene012415, positively correlated with MeSA both in aphid and AM fungus groups. In conclusion, AM fungus increased alfalfa's growth, defense enzyme activities, hormones, and VOCs content and up-regulated VOC-related genes to enhance the alfalfa's resistance following aphid infestation.

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Life table data of the green pea aphid, Acyrthosiphon pisum (Harris) reared on four different resistant alfalfa varieties, i.e., 5S43, TG4 CW044026 (abbreviated as TG4), TG7 CW2883 (abbreviated as TG7), and Aurora were analyzed using the age-stage, two-sex life table. A higher proportion of alate adults were observed on 5S43, TG7, and Aurora; while a higher proportion of apterous adults occurred on TG4. The contributions of alate aphids to the finite rate of increase (λ), intrinsic rate of increase (r), and net reproductive rate (R0) were higher than apterous aphids on 5S43, TG7, and Aurora, while apterous aphids contributed more to λ, r, and R0 on TG4. The highest population parameters were observed on TG4 (r = 0.208 d-1, λ = 1.231 d-1, and R0 = 18.8 offspring/individual), while the lowest values were on TG7 (r = 0.129 d-1, λ = 1.138 d-1, and R0 = 9.9 offspring/individual). Because the age-stage, two-sex life table is capable of describing the stage differentiation, it enables the calculation of the stable stage distribution (SSD). A higher proportion of adult A. pisum was observed in SSD than in fourth instar nymphs. Population simulation showed the stage structure will approach SSD. Because the R0 and the mean generation time (T) values do not reflect the population growth rate, their use as population fitness parameters should be avoided. These findings can be utilized in helping to select resistant alfalfa varieties to effectively manage the pea aphid.

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Aphids on alfalfa (Medicago sativa) including Aphis craccivora Koch (cowpea aphid, CPA), Acyrthosiphon pisum Harris (pea aphid, PA) and Therioaphis trifolii Buckton (spotted alfalfa aphid, SAA) cause significant yield losses worldwide. In this experiment, the development of these three species of aphids on 16 alfalfa cultivars was compared. The results showed that the plant cultivar had a significant influence on the development of aphids as there are significant differences in the body weight of aphids reared on different alfalfa cultivars. In addition, antibiosis between the alfalfa cultivars Pegasis and Gannong NO.9 and the three species of aphids was evaluated by measuring aphid body weight and fecundity. Antixenosis was measured using choice tests, and feeding behavior was quantified using electrical penetration graphs (EPG). The Pegasis cultivar was observed to have both antibiosis and antixenosis effects with CPA, but was susceptible to PA and SAA compared with the Gannong NO.9 cultivar. CPA had less mean body weight, less fecundity, and shorter feeding time on the Pegasis cultivar, and preferred to settle on Gannong NO.9 cultivar. In contrast, Gannong NO.9 exhibits antibiosis and antixenosis to PA and SAA compared with Pegasis, as shown by lower body weight, lower fecundity and chose to settle less often, but EPG data showed that PA and SAA showed no different significance in feeding behavior between Pegasis and Gannong NO.9.

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Host adaptation has the potential to cause rapid genetic variation in symbiotic microorganisms in insects. How mutations in symbiotic viruses favor viral fitness in hosts and even influence host adaptability to new environments remains elusive. Here, we explored the role of genetic divergence at one site of a symbiotic virus, Acyrthosiphon pisum virus (APV), in the host aphid's adaptation to unfavorable plants. Based on the transcriptomes of the pea aphid Vicia faba colony and Vicia villosa colony, 46 single nucleotide polymorphism (SNP) sites were found in the APV genomes from the two aphid colonies. One SNP at site 5,990, G5990A, located at the RNA-dependent RNA polymerase (RdRp) domain, demonstrated a predominance from G to A when the host aphids were shifted from V. faba to the low-fitness plants V. villosa or Medicago sativa. This SNP resulted in a substitution from serine (S) to asparagine (N) at site 196 in RdRp. Although S196N was predicted to be located at a random coil far away from conserved functional motifs, the polymerase activity of the N196 type of RdRp was increased by 44.5% compared to that of the S196 type. The promoted enzymatic activity of RdRp was associated with a higher replication level of APV, which was beneficial for aphids as APV suppressed plant's resistance reactions toward aphids. The findings showed a novel case in which mutations selected in a symbiotic virus may confer a favor on the host as the host adapts to new environmental conditions.

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BACKGROUND: Host-parasite interactions represent complex co-evolving systems in which genetic and associated phenotypic variation within a species can significantly affect selective pressures on traits, such as host immunity, in the other. While often modelled as a two-species interaction between host and parasite, some systems are more complex due to effects of host enemies, intraguild predation, and endosymbionts, all of which affect host immunity. However, it remains unclear how these factors, combined with genetic variation in the host and the parasitoid, affect host immunity. We address this question in an important agricultural pest system, the pea aphid Acyrthosiphon pisum, which shows significant intraspecific variability in immunity to the parasitoid wasp Aphidius ervi. In a complex experiment, we use a quantitative genetic design in the parasitoid, two ecologically different aphid lineages and the aphid lion Chrysoperla carnea as an intraguild predator to unravel the complex interdependencies. RESULTS: We demonstrate that aphid immunity as a key trait of this complex host-parasite system is affected by intraspecific genetic variation in the parasitoid and the aphid, the interaction of intraspecific genetic variation with intraguild predation, and differences in defensive endosymbionts between aphid lineages. Further, aphid lineages differ in their altruistic behaviour whereby infested aphids move away from the clonal colony to facilitate predation. CONCLUSIONS: Our findings provide new insights into the influence of endosymbiosis and genetic variability in an important host-parasitoid system which is influenced by natural enemies of the parasitoid and the aphid, including its endosymbiont communities. We show that endosymbiosis can mediate or influence the evolutionary arms race between aphids and their natural enemies. The outcome of these complex interactions between species has significant implications for understanding the evolution of multitrophic systems, including eco-agricultural settings.

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Introduction: Arbuscular mycorrhizal (AM) fungi are important for the resistance of plants to insect infestation and diseases. However, the effect of AM fungal colonization of plants response to pathogen infection activated by pea aphid infestation is unknown. Pea aphid (Acyrthosiphon pisum) and the fungal pathogen Phoma medicaginis severely limit alfalfa production worldwide. Methods: This study established an alfalfa (Medicago sativa)-AM fungus (Rhizophagus intraradices)-pea aphid-P. medicaginis experimental system to clarify the effects of an AM fungus on the host plant response to insect infestation and subsequent fungal pathogen infection. Results: Pea aphid increased the disease incidence of P. medicaginis by 24.94%. The AM fungus decreased the disease index by 22.37% and enhanced alfalfa growth by increasing the uptake of total nitrogen and total phosphorus. The aphid induced polyphenol oxidase activity of alfalfa, and the AM fungus enhanced plant-defense enzyme activity against aphid infestation and subsequent P. medicaginis infection. In addition, the AM fungus increased the contents of jasmonic acid and abscisic acid in plants exposed to aphid infestation or pathogen infection. Abscisic acid and genes associated with the gene ontology term "hormone binding" were upregulated in aphid-infested or pathogen-infected alfalfa. Discussion: The results demonstrate that an AM fungus enhances plant defense and signaling components induced by aphid infestation, which may contribute to improved defense against subsequent pathogen infection.

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The pea aphid, Acyrthosiphon pisum Harris, is a major pest of alfalfa in northwestern China. However, the roles of different groups of natural enemies in combination with aphid-resistant cultivars in the suppression of the pea aphid have not been clarified under field conditions. In this study, we used experimental cages to better understand the top-down (natural enemies) and bottom-up (nine alfalfa cultivars) biological processes, as well as the individual roles of the two processes, in the control of the pea aphid. There was a significant difference in resistance among cultivar classes revealed when natural enemies were excluded. The functional contribution of top-down suppression was higher than the bottom-up process, with natural enemies significantly suppressing aphid populations, regardless of the resistance level of different alfalfa cultivars. The mean biological efficacies of predators, parasitoids, and mixed populations of natural enemies were 85%, 42%, and 88%, respectively. Overall, our study indicated that natural enemies play a critical role in suppressing aphid populations, especially in the summer, whereas cultivar resistance did not combine effectively with natural enemies to inhibit the growth of aphids. Conservation biological control (CBC) can be implemented in the alfalfa production regions in northwestern China to reduce the overreliance on insecticides for the control of pests and mitigate their harmful effects on humans, ecosystems, and biodiversity.

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Carotenoids are involved in many essential physiological functions and are produced from geranylgeranyl pyrophosphate through synthase, desaturase, and cyclase activities. In the pea aphid (Acyrthosiphon pisum), the duplication of carotenoid biosynthetic genes, including carotenoid synthases/cyclases (ApCscA-C) and desaturases (ApCdeA-D), through horizontal gene transfer from fungi has been detected, and ApCdeB has known dehydrogenation functions. However, whether other genes contribute to aphid carotenoid biosynthesis, and its specific regulatory pathway, remains unclear. In the current study, functional analyses of seven genes were performed using heterologous complementation and RNA interference assays. The bifunctional enzymes ApCscA-C were responsible for the synthase of phytoene, and ApCscC may also have a cyclase activity. ApCdeA, ApCdeC, and ApCdeD had diverse dehydrogenation functions. ApCdeA catalyzed the enzymatic conversion of phytoene to neurosporene (three-step product), ApCdeC catalyzed the enzymatic conversion of phytoene to ζ-carotene (two-step product), and ApCdeD catalyzed the enzymatic conversion of phytoene to lycopene (four-step product). Silencing of ApCscs reduced the expression levels of ApCdes, and silencing these carotenoid biosynthetic genes reduced the α-, ß-, and γ-carotene levels, as well as the total carotenoid level. The results suggest that these genes were activated and led to carotenoid biosynthesis in the pea aphid.

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Aphids are important agricultural pests, vectors of many plant viruses and have sophisticated relationships with symbiotic microorganisms. Abundant asymptomatic RNA viruses have been reported in aphids due to the application of RNA-seq, but aphid-virus interactions remain unclear. Bunyavirales is the most abundant RNA virus order, which can infect mammals, arthropods, and plants. However, many bunyaviruses have specific hosts, such as insects. Here, we discovered 18 viruses from 10 aphid species by RNA-seq. Importantly, a widespread presence bunyavirus, Aphid bunyavirus 1 (ABV-1), was determined to have a wide host range, infecting and replicating in all 10 tested aphid species. ABV-1 may be transmitted horizontally during feeding on plant leaves and vertically through reproduction. In a comparison of the physiological parameters of ABV-1high and ABV-1low strains of pea aphid, higher ABV-1 titers reduced the total nymphal duration and induced the reproduction. Moreover, viral titer significantly affected the lipid and protein contents in pea aphids. In summary, we proposed that ABV-1 may have stable symbiont-like relationships with aphids, and these observations may provide a new direction for studying bunyaviruses in aphids and establishing a model for virus-aphid interactions.

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